Hostname: page-component-7b7567c8c-fvjsw Total loading time: 0 Render date: 2026-11-14T07:44:00.642Z Has data issue: false hasContentIssue false
  • English
  • Français

Parasites and low temperatures

Published online by Cambridge University Press:  16 October 2009

D. A. Wharton
D. A. Wharton
Affiliation:
Department of Zoology, University of Otago, P.O. Box 56, Dunedin, New Zealand
Rights & Permissions [Opens in a new window]

Summary

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the 'Save PDF' action button.

Low temperatures affect the rate of growth, development and metabolism of parasites and when temperatures fall below 0°C may expose the parasite to the potentially lethal risk of freezing. Some parasites have mechanisms, such as diapause, which synchronise their life cycle with favourable seasons and the availability of hosts. Parasites of endothermic hosts are protected from low temperatures by the thermoregulatory abilities of their host. Free-living and off-host stages, however, may be exposed to subzero temperatures and both freezing-tolerant and freeze-avoiding strategies of cold hardiness are found. Parasites of ectothermic hosts may be exposed to subzero temperatures within their hosts. They can rely on the cold tolerance adaptations of their host or they may develop their own mechanisms. Exposure to low temperatures may occur within the carcass of the host and this may be of epidemiological significance if the parasite can be transmitted via the consumption of the carcass.

Keywords

Temperaturefreezingcold tolerancediapause

Information

Type
Research Article
Information
Parasitology , Volume 119 , Supplement S1: Parasite Adaptation to Environmental Constraints , December 1999, pp. S7 - S17
Copyright
Copyright © Cambridge University Press 1999

References

REFERENCES

Allan, G. s. & Wharton, D. A. (1990). Anhydrobiosis in the infective juveniles of Trichostrongylus colubriformis (Nematoda: Trichostrongylidae). International Journal for Parasitology 20, 183–192.Google Scholar
Antoniou, M. (1989). Arrested development in plant parasitic nematodes. Helminthological Abstracts B58, 1–19.Google Scholar
Asahina, E. (1959). Frost-resistance in a nematode, Aphelenchoides ritzema-bosi. Low Temperature Science B17, 51–62.Google Scholar
Ash, C. P. J & Atkinson, H. J. (1983). Evidence for a temperature-dependent conversion of lipid reserves to carbohydrate in quiescent eggs of the nematode, Nematodirus battus. Comparative Biochemistry and Physiology 76B, 603–610.Google Scholar
Ash, C. P. J. & Atkinson, H. J. (1986). Nematodirus battus: development of cold hardiness in dormant eggs. Experimental Parasitology 62, 24–28.CrossRefGoogle ScholarPubMed
Bale, J. s. (1993). Classes of insect cold hardiness. Functional Ecology 7, 751–753.Google Scholar
Bartlett, L. M. (1992). Cold-hardiness in Pelecitus fulicaeatrae (Nematoda: Filarioidea), a parasite in the ankle of Fulica americana (Aves). Journal of Parasitology 78, 138–139.CrossRefGoogle ScholarPubMed
Block, w. (1995). Insects and freezing. Science Progress 78, 349–372.Google Scholar
Block, W., Turnock, W. J. & Jones, T. H. (1987). Cold resistance and overwintering survival of the cabbage root fly, Delia radicum (Anthomyiidae), and its parasitoid, Trybliographa rapae (Cynipidae), in England. Oecologia 71, 332–338.CrossRefGoogle ScholarPubMed
Brown, I. M. & Gaugler, R. (1996). Cold tolerance of steinernematid and heterorhabditid nematodes. Journal of Thermal Biology 21, 115–121.CrossRefGoogle Scholar
Brown, I. M. & Gaugler, R. (1998). Survival of steinernematid nematodes exposed to freezing. Journal of Thermal Biology 23, 75–80.Google Scholar
Burks, C. S., Stewart, R. L., Needham, G. R. & Lee, R. E. (1996). The role of direct chilling injury and inoculative freezing in cold tolerance of Amblyomma americanum, Dermacentor variabilis and Ixodes scapularis. Physiological Entomology 21, 44–50.Google Scholar
Clarke, A. J. & Hennessy, J. (1976). The distribution of carbohydrates in cysts of Heterodera rostochiensis. Nematologica 22, 190–195.Google Scholar
Cross, D. A., Klesius, P. H. & Williams, J. C. (1988). Preliminary report: immunodiagnosis of pre-type II ostertagiasis. Veterinary Parasitology 27, 151–158.CrossRefGoogle ScholarPubMed
Dautel, H. & Knulle, W. (1997). Cold hardiness, supercooling ability and causes of low-temperature mortality in the soft tick, Argas reflexus, and the hard tick, Ixodes ricinus (Acari, Ixodoidea) from Central Europe. Journal of Insect Physiology 43, 843–854.Google Scholar
Davenport, J. (1992). Animal Life at Low Temperature. New York and London: Chapman and Hall.Google Scholar
Duman, J. G., Xu, L., Neven, L. G., Thursman, D. & Wu, D. w. (1991). Hemolymph proteins involved in insect subzero-temperature tolerance: ice nucleators and antifreeze proteins. In Insects at Low Temperatures (ed. Lee, R. E. & Denlinger, D. L.), pp. 94–127. New York and London: Chapman and Hall.Google Scholar
Evans, A. A. F (1987). Diapause in nematodes as a survival strategy. In Vistas on Nematology (ed. Veech, J. A. & Dickson, D. W.), pp. 180–187. Hyattsville, Maryland: Society of Nematologists Inc.Google Scholar
Evans, A. A. F & Peery, R. N. (1976). Survival strategies in nematodes. In The Organisation of Nematodes (ed. Croll, N. A.), pp. 383–424. London & New York: Academic Press.Google Scholar
Eveleigh, E. S. & Threlfall, w. (1974). The biology of Ixodes (Ceratixodes) uriae White, 1852 in Newfoundland. Acarologia 16, 621–635.Google Scholar
Eysker, M. (1997). Some aspects of inhibited development of trichostrongylids in ruminants. Veterinary Parasitology 72, 265–283.Google Scholar
Forge, T. A. & MacGumwin, A. E. (1990). Cold hardening of Meloidogyne hapla second-stage juveniles. Journal of Nematology 22, 101–105.Google ScholarPubMed
Forge, T. A. & MacGumwin, A. E. (1992 a). Impact of thermal history on tolerance of Meloidogyne hapla second-stage juveniles to external freezing. Journal of Nematology 24, 262–268.Google Scholar
Forge, T. A. & MacGumwin, A. E. (1992 b). Effects of water potential and temperature on survival of the nematode Meloidogyne hapla in frozen soil. Canadian Journal of Zoology 70, 1553–1560.CrossRefGoogle Scholar
Friedman, M. J. (1990). Commercial production and development. In Entomopathogenic Nematodes in Biological Control (ed. Gaugler, R. & Kaya, H. K.), pp. 153–172. Boca Raton: CRC Press.Google Scholar
Gibbs, H. c. (1986). Hypobiosis in parasitic nematodes – an update. Advances in Parasitology 25, 129–174.CrossRefGoogle ScholarPubMed
Gustafson, P. V. (1953). The effect of freezing on encysted Anisakis larvae. Journal of Parasitology 39, 585–588.Google Scholar
Hance, T. & Boivin, G. (1993). Effect of parasitism by Anaphes sp. (Hymenoptera, Mymaridae) on the cold hardiness of Listronotus oregonensis (Coleoptera, Curculionidae) eggs. Canadian Journal of Zoology 71, 759–764.CrossRefGoogle Scholar
Hominick, w. M. (1986). Photoperiod and diapause in the potato cyst-nematode, Globodera rostochiensis. Nematologica 32, 408–418.CrossRefGoogle Scholar
Horwarth, K. C. & Duman, J. G. (1984). Yearly variations in the overwintering mechanisms of the cold-hardy beetle, Dendroides canadensis. Physiological Zoology 57, 40–45.Google Scholar
Humble, L. M. & Ring, R. A. (1985). Inoculative freezing of a larval parasitoid within its host. Cryo-Letters 6, 59–66.Google Scholar
Jones, P. W., Tylka, G. L. & Perry, R. N. (1998). Hatching. In The Physiology and Biochemistry of Free-living and Plant-parasitic Nematodes (ed. Perry, R. N. & Wright, D. J.), pp. 181–212. Walhngford & New York: CABI Publishing.Google Scholar
Kapel, C. M. O, Pozio, E., Sacchi, L. & Presturd, P. (1999). Freeze tolerance, morphology, and RAPD-PCR identification of Trichinella nativa in naturally infected arctic foxes. Journal of Parasitology 85, 144–147.Google Scholar
Karlsson, J. O. M, Cravalho, E. G. & Toner, M. (1993). Intracellular ice formation: causes and consequences. Cryo-Letters 14, 323–336.Google Scholar
Kennedy, c. R. (1975). Ecological Animal Parasitology. Oxford: Blackwell Scientific Publications.Google Scholar
Knight, C. A. & Duman, J. G. (1986). Inhibition of recrystallization of ice by insect thermal hysteresis proteins: a possible cryoprotective role. Cryobiology 23, 256–262.CrossRefGoogle Scholar
Lackie, A. M. (1975). The activation of infective stages of endoparasites of vertebrates. Biological Reviews 50, 285–323.CrossRefGoogle ScholarPubMed
Layne, J. R. & Lee, R. E. (1995). Adaptations of frogs to survive freezing. Climate Research 5, 53–59.CrossRefGoogle Scholar
Lee, R. E. (1991). Principles of insect low temperature tolerance. In Insects at Low Temperatures (ed. Lee, R. E. & Denlinger, D. L.), pp. 17–46. New York and London: Chapman and Hall.Google Scholar
Lee, R. E. & Baust, J. G. (1987). Cold-hardiness in the Antarctic tick, Ixodes uriae. Physiological Zoology 60, 499–506.CrossRefGoogle Scholar
Lee, R. E. & Costanzo, J. p. (1998). Biological ice nucleation and ice distribution in cold-hardy ectothermic animals. Annual Review of Physiology 60, 55–72.CrossRefGoogle ScholarPubMed
Lorentzen, G. & Halvorsen, o. (1986). Survival of the first stage larva of the metastrongylid nematode Elaphostrongylus rangiferi under various conditions of temperature and humidity. Holoarctic Ecology 9, 301–304.Google Scholar
Mcallister, C. T., Upton, S. J., Trauth, S. E. & Bursey, c. R. (1995). Parasites of Wood Frogs, Rana sylvatica (Ranidae), from Arkansas, with a description of a new species of Eimeria (Apicomplexa, Eimeriidae). Journal of the Helminthological Society of Washington 62, 143–149.Google Scholar
Mcgrath, J. J. (1987). Cold shock: thermoelastic stress in chilled biological membranes. In Network Thermodynamics, Heat and Mass Transfer in Biotechnology (ed. Diller, K. R.), pp. 57–66. New York: United Engineering Center.Google Scholar
Miller, p. M. (1968). The susceptibility of parasitic nematodes to sub-freezing temperatures. Plant Disease Reporter 52, 768–772.Google Scholar
Needham, G. R. & Teal, P. D. (1991). Off-host physiological ecology of ixodid ticks. Annual Review of Entomology 36, 659–681.Google Scholar
Popiel, i. & Vasquez, E. M. (1991). Cryopreservation of Steinernema carpocapsae and Heterorhabditis bacteriophora. Journal of Nematology 23, 432–437.Google Scholar
Poulin, R. (1998). Evolutionary Ecology of Parasites – From Individuals to Communities. London: Chapman & Hall.Google Scholar
Pullin, A. s. (1994). Cold tolerance of an insect parasitoid Cotesia (apanteles) glomeratus and a comparison with that of its host Pieris brassicae and a hyperparasitoid Testrastichus galactopus. Cryo-Letters 15, 67–74.Google Scholar
Quinn, P. J. (1985). A lipid-phase separation model of low-temperature damage to biological membranes. Cryobiology 22, 128–146.Google Scholar
Ramlov, H., Bedford, J. & Leader, J. (1992). Freezing tolerance of the New Zealand alpine weta, Hemideina maori Hutton (Orthoptera; Stenopelmatidae). Journal of Thermal Biology 17, 51–54.CrossRefGoogle Scholar
Rogers, w. p. (1960). The physiology of the infective process of nematode parasites: the stimulus from the animal host. Proceedings of the Royal Society of London B152, 367–386.Google Scholar
Rubinsky, B., Wong, S. T. S, Hong, J. S., Gillbert, J., Roos, M. & Storey, K. B. (1994). 1H magnetic resonance imaging of freezing and thawing in freeze-tolerant frogs. American Journal of Physiology 266, R1771–1777.Google ScholarPubMed
Sayre, R. M. (1964). Cold-hardiness of nematodes. I. Effects of rapid freezing on the eggs and larvae of Meloidogyne incognita and M. hapla. Nematologica 10, 168–179.Google Scholar
Sinclair, B. J. (1997). Seasonal variation in freezing tolerance of the New Zealand alpine cockroach Celatoblatta quinquemaculata. Ecological Entomology 22, 462–467.CrossRefGoogle Scholar
Sinclair, B. J., Worland, M. R. & Wharton, D. A. (1999). Ice nucleation and freezing tolerance in New Zealand alpine and lowland weta, Hemideina spp. (Orthoptera; Stenopelmatidae). Physiological Entomology 24, 56–63.Google Scholar
Smith, H. J. (1984). Preconditioning of Trichinella spiralis nativa larvae in musculature to low temperatures. Veterinary Parasitology 17, 85–90.Google Scholar
Smith, H. J. (1987). Factors affecting preconditioning of Trichinella spiralis nativa larvae in musculature to low temperatures. Canadian Journal of Veterinary Research 51, 169–173.Google Scholar
Spratt, D. M. (1972). Aspects of the life cycle of Dirofilaria raemeri in naturally and experimentally infected kangaroos, wallaroos and wallabies. International Journal for Parasitology 2, 139–156.Google Scholar
Storey, K. B. & Storey, J. M. (1988). Freeze tolerance in animals. Physiological Reviews 68, 27–84.CrossRefGoogle ScholarPubMed
Storey, K. B. & Storey, J. M. (1996). Natural freezing survival in animals. Annual Review of Ecology and Systematics 27, 365–386.Google Scholar
Sullivan, C. R., Griffiths, K. J. & Wallace, D. R. (1977). Low winter temperatures and the potential for establishment of the egg parasite Anastatus disparis (Hymenoptera: Eupelmidae) in Ontario populations of the gypsy moth. The Canadian Entomologist 109, 215–220.Google Scholar
Surrey, M. R. (1996). The effect of rearing method and cool temperature acclimation on the cold tolerance of Heterorhabditis zealandica infective juveniles (Nematoda: Heterorhabditidae). Cryo-Letters 17, 313–320.Google Scholar
Thomas, R. J. (1974). The role of climate in the epidemiology of nematode parasitism in ruminants. In The Effects of Meteorological Factors Upon Parasites (ed. Taylor, A. E. R & Muller, R.), pp. 13–32. Oxford: Blackwell.Google Scholar
Turnock, w. J. & Bilodeau, R. J. (1992). Life history and coldhardiness of Athrycia cinerea (Dipt.: Tachinidae) in western Canada. Entomophaga 37, 353–362.CrossRefGoogle Scholar
Tyrrell, C., Wharton, D. A., Ramlov, H. & Moller, H. (1994). Cold tolerance of an endoparasitic nematode within a freezing tolerant orthopteran host. Parasitology 109, 367–372.Google Scholar
Vannier, G. (1994). The thermobiological limits of some freezing intolerant insects: The supercooling and thermostupor points. Acta Oecologica 15, 31–42.Google Scholar
Wertejuk, M. (1959). Influence of environmental temperature on the invasive larvae of gastrointestinal nematodes of sheep. Acta Parasitologica Polonica 7, 315–342.Google Scholar
Wharton, D. A. (1986). A Functional Biology of Nematodes. London & Sydney: Croom Helm.Google Scholar
Wharton, D. A. (1995). Cold tolerance strategies in nematodes. Biological Reviews 70, 161–185.CrossRefGoogle ScholarPubMed
Wharton, D. A. & Allan, G. S. (1989). Cold tolerance mechanisms of the free-living stages of Trichostrongylus colubriformis (Nematoda: Trichostrongylidae). Journal of Experimental Biology 145, 353–370.CrossRefGoogle Scholar
Wharton, D. A., Perry, R. N. & Beane, J. (1993). The role of the eggshell in the cold tolerance mechanisms of the unhatched Juveniles of Globodera rostochiensis. Fundamental and Applied Nematology 16, 425–431.Google Scholar
Wharton, D. A. & Ramløv, H. (1995). Differential scanning calorimetry studies on the cysts of the potato cyst nematode Globodera rostochiensis during freezing and melting. Journal of Experimental Biology 198, 2551–2555.Google Scholar
Wharton, D. A. & Surrey, M. R. (1994). Cold tolerance mechanisms of the infective larvae of the insect parasitic nematode, Heterorhabditis zealandica Poinar. Cryo-Letters 25, 749–752.Google Scholar
Wharton, D. A. & To, N. B. (1996). Osmotic stress effects on the freezing tolerance of the Antarctic nematode Panagrolaimus davidi. Journal of Comparative Physiology B166, 344–349.Google Scholar
Wharton, D. A., Young, S. R. & Barrett, J. (1984). Cold tolerance in nematodes. Journal of Comparative Physiology B154, 73–77.Google Scholar
Whitehead, M. D., Burton, H. R., Bell, P. J., Arnould, J. P. Y. & Rounsevell, D. E. (1991). A further contribution on the biology of the Antarctic flea, Glaciopsyllus antarcticus (Siphonaptera, Ceratophyllidae). Polar Biology 11, 379–383.Google Scholar
Woodhams, D. C., Costanzo, J. P., Kelty, J. D. & Lee, R. E. (2000). Cold hardiness in two helminth parasites of the freeze tolerant wood frog, Rana sylvatica. Canadian Journal of Zoology (in press).CrossRefGoogle Scholar
Womersley, C. Z. (1990). Dehydration survival and anhydrobiotic survival. In Entomopathogenic Nematodes in Biological Control (ed. Gaugler, R. & Kaya, H. K.) pp. 117–137. Boca Raton: CRC Press.Google Scholar
Womersley, C. Z., Wharton, D. A. & Higa, L. M. (1998). Survival biology. In The Physiology and Biochemistry of Free-living and Plant-parasitic Nematodes (ed. Perry, R. N. & Wright, D. J.), pp. 271–302. Wallingford & New York: CABI Publishing.Google Scholar
Yoder, H. R. & Coggins, J. R. (1996). Helminth communities in the Northern Spring Peeper, Pseudacris c. crucifer Wied, and the Wood Frog, Rana sylvatica Le Conte, from Southeastern Wisconsin. Journal of the Helminthological Society of Washington 63, 211–214.Google Scholar
Zachariassen, K. A. (1985). Physiology of cold tolerance in insects. Physiological Reviews 65, 799–832.Google Scholar